How the Brain Might Work: A New Theory of Consciousness

FOR scientists who study the human brain, even its simplest act of perception is an event of astonishing intricacy.

Consider this: It is a beautiful spring day and you are walking down a country lane, absorbed in thought. Birds are chirping, roses are in bloom and the sun feels warm on your face. Suddenly, you hear a dog bark and you switch your attention to seeing if the animal means to bite.

Years of research have shown that the brain absorbs a scene like this by carving it into components and analyzing each chunk of information along separate pathways. As the eyes gaze at the rose, it is not the whole image of the rose that is transmitted to the brain. Instead, something very puzzling takes place. The nerve cells in the retina immediately break down the image into separate components, like its contours, textures and colors. As the ear hears birds chirping, separate cells respond to each frequency while others compute the direction and intensity of the sound. Cells in the skin that respond to warmth channel their input to yet another part of the brain.

Each population of sensory cells, from the eye, ear, nose and skin, sends its information to its home area on the outer surface of the brain, a thin, deeply furrowed sheet of cells known as the cerebral cortex.

The sensations of one instant of a spring morning have thus become represented by millions of activated cells in many different regions of the cortex. That much is known. A still baffling question for scientists is, how does the brain bind these fragmented pieces of information into a single coherent image? The nature of the reassembly process, known as the binding problem, is intimately related to the age-old question of consciousness, since an answer to the binding problem would go far to defining the physical basis of the conscious mind.

The first step to understanding, brain scientists say, is to realize that there is no Cinemascope screen in the brain where all the pieces come together. But if there is no screen, on what physical principle is consciousness organized? A growing number of scientists say the answer must lie in some form of timing. An image may be reconstructed from all cells that are firing in a particular rhythm at a particular instant.

Recent experiments have shown that precise timing codes are the brain's primary organizing principle, at least at the level of individual neurons, among specialized groups of neurons and across different parts of the brain.

But exactly how the timing codes work is a matter of vigorous debate. "Cells do carry information by virtue of the fact that they are firing at the same time," said Dr. Nancy Kopell, a biologist at Brandeis University in Waltham, Mass., who studies how creatures move. "But what this means for function is unclear." Different solutions proposed for the binding problem have produced a lot of "yelling and screaming," Dr. Kopell said.

Nevertheless, efforts to understand how the brain uses time are forging ahead, said Dr. Christof Koch, a neuroscientist at the California Institute of Technology in Pasadena who is a leading theorist on the nature of human consciousness. The challenge is to construct theories "firmly based on nerve cells, their firing properties and their anatomical connections," he said. The brain may have evolved different binding solutions for different levels of organization.

The search for timing codes gets more speculative at the level of cell populations, Dr. Koch said. The basic idea is that cells involved in forming a perception will fire simultaneously, thus binding together in time rather than space. Every perception would be based on the temporary activation of an ensemble of neurons, he said. When a new perception is formed, the previous ensemble falls away and a new grouping of neurons fires, forming a new perception. Single neurons can participate in the representation of many things, depending on the ensembles they join in any one instant.

At the University of California at Davis, Dr. Charles Gray is recording the electrical activity of brain cells in different parts of the monkey visual system. There is a growing amount of evidence that cells fire in synchrony, he said. The problem is knowing if such synchrony is related to behavior -- something no one has yet proved.

And even if cells fire synchronously, which cells are they? Is there something special about them? Dr. Gyorgy Buzsaki, a neuroscientist at Rutgers University in Newark, N.J., thinks there is. He has found that a class of cells called inhibitory interneurons have an inherent tendency to fire in a wavelike pattern. From the way they are distributed in the brain, these neurons could perform a binding function, he said.

"You can compare it to traffic control in New York City," Dr. Buzsaki said. "Say you have an imaging device that looks at 5,000 vehicles -- cars, trucks, taxis, bicycles -- all moving together in chunks. You'd like to figure out how they interact to achieve this togetherness. One answer is traffic lights," he said. Like traffic lights, interneurons are rhythmic and well coordinated and could control the flow of cognition. When interneurons are damaged, he said, the result is epilepsy -- a storm of uncoordinated electrical activity in the brain.

Different brain regions may have evolved their own temporal binding codes, said Dr. Rodolfo Llinas, a professor of neuroscience at New York University. The motor system is a good example. The cerebellum is a structure that coordinates movements, relaying a barrage of signals from higher brain regions where decisions are made to the muscles. How is this coordination achieved?

The brain stem contains a nucleus of cells that burst at a rate of 10 cycles per second. These cells, inferior olivary neurons, send long fibers up to the cerebellum, where they make dense connections, thus amplifying their signals. Information flowing into the cerebellum is regulated by these bursting cells, making sure that movements only occur 10 times a second, Dr. Llinas said. The oscillation literally binds brain commands with muscle movements.

"This means we move in a noncontinuous manner," Dr. Llinas said. "No one can move faster than 10 times a second because that is the normal frequency we all have. We have the impression of fluidity of motion because it all happens so fast." By binding packets of motor nerve information every tenth of a second, he said, the system has time to send messages to muscles more or less synchronously. The dynamic rhythm allows different combinations of muscles to be used for movements.

The same kind of binding mechanism may exist for the entire brain at a faster frequency of 40 cycles per second, Dr. Llinas said. At New York University he and a colleague, Dr. Urs Ribary, have measured such signals in human brains using a machine that detects magnetic fields on the scalp. The 40-cycle-per-second wave continuously sweeps the brain from front to back every 12.5-thousandth of a second, Dr. Llinas said, and could be the binding signal that links information from the parts of the cortex that handle auditory, visual, motor and other sensory signals.

Dr. Llinas believes that the 40-cycle-per-second wave serves to connect structures in the cortex, where advanced information processing occurs, and the thalamus, a lower brain region where complex relay and integrative functions are carried out. He, too, has a candidate population of cells -- the intralaminar nucleus in the thalamus -- that might generate the binding signal.

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The intralaminar nucleus, a kind of doughnut of cells within the thalamus, is an intriguing structure. Its nerve cells send out long axons that reach to every part of the cerebral cortex. Significantly, there are also returning axons that come down from all areas of the cortex back to the intralaminar nucleus. The thalamus and the cortex are thus connected in a special way.

Intralaminar cells fire in a natural pattern of 40 cycles per second, Dr. Llinas said, and he believes it is their firing rhythm that is the source of the rhythmicity he detects at the surface of the cortex. His idea is that in each cycle a wave of nervous impulses radiates out from around the intralaminar nucleus to all parts of the cortex above, much like the central arm of an old-fashioned radar screen illuminates each object in its path.

The thalamus has another important connection with the cortex, which is that all the body's sensory systems send their inputs to relay stations of nerve cells and then to their own regions of the cortex. All these relay stations are located within the thalamus, which is able to influence their firing patterns. As visual signals come in from the eye, the thalamus insures that active cells in the visual cortex are coordinated into a rhythm of electrical activity that is at or near 40 cycles a second.

Critical to the act of cognition, in Dr. Llinas's theory, is the interaction between the two systems of electrical activity, the active sensory cells in the cortex and the scanning wave from the thalamus. The way the brain creates images, in his view, is as follows. The wave of impulses from around the thalamus's intralaminar nucleus polls all the sensory regions mapped out across the cerebral cortex once every 12.5-thousandth of a second. The regions that have active cells, representing some sensory input, are entrained to the same rhythm as the scanning wave, and send back a train of nervous impulses to the thalamus, all precisely timed in a coherent pattern.

All the coherent impulses that are received in a given cycle are perceived as a single image, Dr. Llinas suggests. The sensory messages of sight, sound, smell and touch, are thus bound together not in a single place but in a single instant of time, Dr. Llinas suggests. When the eye no longer sees an object, those cells no longer respond to the thalamus's scanning system. Each scan -- 12.5-thousandth of a second in length -- creates a new image, but the images come so quickly that they seem continuous, as do the frames of a movie.

The brain has several natural oscillatory states, which correspond to deeply engrained functional states, Dr. Llinas said. For example, when thalamic cells reverberate at two cycles per second, the brain is in a state of deep sleep. At 10 cycles per second, the human brain is awake but not paying attention to the outside world. And at 40 cycles per second it is either wide awake or vividly dreaming.

In walking down the sunny path, absorbed in thought, a person would be generating regular 40-cycle-per-second rhythms while constructing internal images of the external world, according to Dr. Llinas's theory. As long as the internal images agree with what is happening outside, the brain keeps updating the scene with a steady rhythm.

But when the dog barks, posing a threat, the 40-cycle-per-second signal is abruptly reset so as to incorporate the novel stimulus into the overall scene so that the new information can be dealt with.

Dr. Llinas's theory, if true, would resolve the binding problem and also go far to explaining the nature of consciousness. Consciousness is the dialogue between the thalamus and the cerebral cortex. The brain is an organ, and its function is to create images. At night, these images are dreams; during wakefulness, the images are modulated by the senses and represent the outside world to which they correspond in some very practical way that has been determined by evolution. A person's waking life is a dream guided by the senses, Dr. Llinas said.

Dr. Llinas's theory rests on his measurements of various electrical rhythms in the brain, as well as observations such as that when the intralaminar nucleus is damaged, people fall into a deep coma. The critical 40-cycle-per-second rhythm he has measured at the surface of the cerebral cortex had not until recently been detected by others. Such waves could be noise rather than a mechanism for temporal binding, said Dr. Chris Wood, an expert on brain imaging at the Los Alamos National Laboratory in New Mexico.

But Dr. Llinas's theory has received strong support from recent experiments conducted by Dr. Mircea Steriade at the Laval University School of Medicine in Quebec. He and his colleagues implanted electrodes into interconnected areas of a cat's thalamus and cortex, such as the eye's relay station in the thalamus and in the visual cortex.

When the animals were wide awake or dreaming, Dr. Steriade said, cells in both areas would oscillate together at 40 cycles per second for just a brief period. The shared rhythm quickly appears and disappears, he said, which is why others have found it hard to detect.

Dr. Steriade said that in his view the 40-cycle-per-second rhythms "exist spontaneously when animals are in active states of vigilance."

Other neuroscientists are withholding judgment on theories like Dr. Llinas's until the various rhythms or oscillations of nerve cells in the brain are better understood. "There is no question that oscillations exist," said Dr. David Hubel, a leading expert on vision at Harvard Medical School. "But we have no idea what, if anything, they are doing" in the human brain. One can think about temporal coding, he said, "but it's very hard to drum up experiments that get at the problem.

"One has to grant that of the 200 possible cortical areas in the brain, very few have been explored in detail," Dr. Hubel explained. Thus there could be as yet undiscovered, highly specific areas in the brain where information comes together and is bound into a unitary experience.

"No one in neuroscience thinks time is not important," said Dr. Patricia Churchland, a philosopher and brain scientist at the University of California at San Diego. "Criticisms arise with how time management is achieved." Theories like those proposed by Dr. Llinas are an excellent entry into the binding problem, she said, but "do not yet solve the problem."

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A version of this article appears in print on March 21, 1995, on Page C00001 of the National edition with the headline: How the Brain Might Work: A New Theory of Consciousness. Order Reprints|Today's Paper|Subscribe